The Vestibular System

Airplanes and submarines navigate in three dimensions using sophisticated guidance systems that register every acceleration and turn. Laser gyroscopes and computers make these navigational aids extremely precise. Yet the principles of inertial guidance are ancient: Vertebrates have used analogous systems for 500 million years and invertebrates for still longer.

In vertebrates the inertial guidance system is the vestibular system, comprising five sensory organs in the internal ear that measure linear and angular acceleration of the head. Acceleration of the head deflects hair bundles protruding from the hair cells in the inner ear; this distortion changes the cells’ membrane potential, altering the synaptic transmission between the cells and the sensory neurons that innervate them. The signals from these vestibular neurons convey information on head velocity and acceleration to vestibular nuclei in the brain stem.

This information keeps the eyes still when the head moves, helps to maintain upright posture, and influences how we perceive our own movement and the space around us by providing a measure of the gravitational field in which we live. In this chapter we describe how the hair cells of the inner ear generate the signals for head acceleration and how these signals are integrated with other sensory information in the brain.

The Vestibular Apparatus in the Inner Ear Contains Five Receptor Organs

Vestibular signals originate in the labyrinths of the internal ear (Figure 40–1). The bony labyrinth is a hollow structure within the petrous portion of the temporal bone. Within it lies the membranous labyrinth, which contains sensors for both the vestibular and auditory systems.

Figure 40–1 The vestibular apparatus of the inner ear.

A. The orientations of the vestibular and cochlear divisions of the inner ear are shown with respect to the head.

B. The inner ear is divided into bony and membranous labyrinths. The bony labyrinth is bounded by the petrous portion of the temporal bone. Lying within this structure is the membranous labyrinth, which contains the receptor organs for hearing (the cochlea) and equilibrium (the utricle, saccule, and semicircular canals). The space between bone and membrane is filled with perilymph, whereas the membranous labyrinth is filled with endolymph. Sensory cells in the utricle, saccule, and ampullae of the semicircular canals respond to motion of the head. (Adapted, with permission, from Iurato 1967.)

The membranous labyrinth is filled with endolymph, a Na⁺-poor, K⁺-rich fluid whose composition is maintained by the action of ion pumps in specialized cells. Surrounding the membranous labyrinth, in the space between the membranous labyrinth and the wall of the bony labyrinth, is perilymph. Perilymph is a high-Na⁺, low-K⁺ fluid similar in composition to cerebrospinal fluid, with which it is in communication through the cochlear aqueduct. The endolymph and perilymph are kept separate by a junctional complex that girdles the apex of each cell.

During development the labyrinth progresses from a simple sac to a complex of interconnected sensory organs but retains the same fundamental topological organization. Each organ originates as an epithelium-lined pouch that buds from the otic cyst, and the endolymphatic spaces within the several organs remain continuous in the adult. The endolymphatic spaces of the vestibular labyrinth are also connected to the cochlear duct through the ductus reuniens (Figure 40–1B).

The vestibular portion of the labyrinth, or vestibular apparatus, lies posterior to the cochlea and consists of five sensory structures. Three semicircular canals (horizontal, also called lateral; anterior, also called superior; and posterior) sense head rotations, whereas two otolith organs (utricle and saccule) sense linear motion (also called translation). Because gravity is a linear acceleration, the otolith organs also sense the orientation, or tilt, of the head relative to gravity.

Hair Cells Transduce Mechanical Stimuli into Receptor Potentials

Each of the five receptor organs has a cluster of hair cells responsible for transducing head motion into vestibular signals. Angular or linear acceleration of the head leads to a deflection of the hair bundles in a particular group of hair cells of the appropriate receptor organ (Figure 40–2).

Figure 40–2 Hair cells in the vestibular labyrinth transduce mechanical stimuli into neural signals. At the apex of each cell is a hair bundle, the stereocilia of which increase in length toward a single kinocilium. The membrane potential of the receptor cell depends on the direction in which the hair bundle is bent. Deflection toward the kinocilium causes the cell to depolarize and thus increases the rate of firing in the afferent fiber. Bending away from the kinocilium causes the cell to hyperpolarize, thus decreasing the afferent firing rate. (Adapted, with permission, from Flock 1965.)

Vestibular signals are carried from the hair cells to the brain stem by branches of the vestibulocochlear nerve (cranial nerve VIII). Cell bodies of the vestibular nerve are located in the vestibular ganglia of Scarpa within the internal auditory canal (Figure 40–1A). The superior vestibular nerve innervates the horizontal and anterior canals and the utricle, whereas the inferior vestibular nerve innervates the posterior canal and the saccule. The labyrinth’s vascular supply, which arises from the anterior inferior cerebellar artery, mirrors its innervation: The anterior vestibular artery supplies the structures innervated by the superior vestibular nerve, and the posterior vestibular artery supplies the structures innervated by the inferior vestibular nerve.

Like most other hair cells, those of the human vestibular system receive efferent inputs from the brain stem. Although the effect of these inputs has not been extensively studied by recording from hair cells in situ, stimulation of the fibers from the brain stem changes the sensitivity of the afferent axons from the hair cells. Stimulation decreases the excitability of some hair cells, as would be expected if activation of the efferent fibers elicited inhibitory postsynaptic potentials in hair cells. In other hair cells, however, activation of the efferent fibers increases excitability.

Given that hair cells are essentially strain gauges (see Chapter 30), the key to grasping how the vestibular organs operate is to understand how mechanical stimuli are delivered to the constituent hair cells. Distinctive mechanical linkages in the otolith organs and semicircular canals account for the contrasting sensitivities of the two types of vestibular organs.

The Semicircular Canals Sense Head Rotation

An object undergoes angular acceleration when its rate of rotation about an axis changes. The head therefore undergoes angular acceleration when it turns or tilts, when the body rotates, and during active or passive locomotion. The three semicircular canals of each vestibular labyrinth detect these angular accelerations and report their magnitudes and orientations to the brain.

Each semicircular canal is a roughly semicircular tube of membranous labyrinth extending from the utricle. One end of each canal is open to the utricle whereas at the other end, the ampulla, the entire lumen of the canal is traversed by a gelatinous diaphragm, the cupula. The cupula is attached to the epithelium along the perimeter and numerous hair bundles insert into the cupula (Figure 40–3).

Figure 40–3 The ampulla of a semicircular canal.

A. A thickened zone of epithelium, the ampullary crista, contains the hair cells. The hair bundles of the hair cells extend into a gelatinous diaphragm, the cupula, which stretches from the crista to the roof of the ampulla.

B. The cupula is displaced by the flow of endolymph when the head moves. As a result, the hair bundles are also displaced. Their movement is greatly exaggerated in the diagram.

The vestibular organs detect accelerations of the head because the inertia of their internal contents results in forces on their hair cells. Consider the simplest situation, a rotation in the plane of a semicircular canal. When the head begins to rotate, the membranous and bony labyrinths move along with it. Because of its inertia, however, the endolymph lags behind the surrounding membranous labyrinth, thus rotating within the canal in a direction opposite that of the head.

The motion of endolymph in a semicircular canal can be demonstrated with a cup of coffee. While gently twisting the cup about its vertical axis, observe a particular bubble near the fluid’s outer boundary. As the cup begins to turn, the coffee tends to maintain its initial orientation in space and thus counter-rotates in the vessel. If you continue rotating the cup at the same speed, the coffee (and the bubble) eventually catch up to the cup and rotate with it. When the cup decelerates and stops, the coffee keeps rotating, moving in the opposite direction relative to the cup.

In the ampulla this relative motion of the endolymph creates pressure on the cupula, bending it toward or away from the adjacent utricle, depending on the direction of endolymph flow. The resulting deflection of the stereocilia alters the membrane potential of the hair cells, thereby changing the firing rates of the associated sensory fibers. The stereocilia are arranged so that endolymph flow toward the cupula is excitatory for the horizontal canals, whereas flow away from the cupula is excitatory for the anterior and posterior vertical canals.

Each semicircular canal is maximally sensitive to rotations in its plane. The horizontal canal is oriented roughly in the horizontal plane, rising slightly from posterior to anterior, and thus is most sensitive to rotations in the horizontal plane. The anterior and posterior canals are oriented more vertically, approximately 45 degrees from the sagittal plane (Figure 40–4).

Figure 40–4 The bilateral symmetry of the semicircular canals. The horizontal canals on both sides lie in approximately the same plane and therefore are functional pairs. The bilateral vertical canals have a more complex relationship. The anterior canal on one side and the posterior canal on the opposite side lie in parallel planes and therefore constitute a functional pair.

Because there is approximate mirror symmetry of the left and right labyrinths, the six canals effectively operate as three coplanar pairs. The two horizontal canals form one pair; each of the other pairs consists of one anterior canal and the contralateral posterior canal. The canal planes are also roughly the pulling planes of the eye muscles. The pair of horizontal canals lies in the pulling plane of the lateral and medial rectus muscles. The left anterior and right posterior pair lies in the pulling plane of the left superior and inferior rectus and right superior and inferior oblique muscles. The right anterior and left posterior pair occupies the pulling plane of the left superior and inferior oblique and right superior and inferior rectus muscles.

The Otolith Organs Sense Linear Accelerations

The vestibular system must compensate not only for head rotations but also for linear motion. The two otolith organs, the utricle and saccule, detect linear motion as well as the static orientation of the head relative to gravity, which is itself a linear acceleration. Each organ consists of a sac of membranous labyrinth approximately 3 mm in the longest dimension. The hair cells of each organ are arranged in a roughly elliptical patch called the macula. The human utricle contains approximately 30,000 hair cells, whereas the saccule contains some 16,000.

The hair bundles of the otolithic hair cells extend into a gelatinous sheet, the otolithic membrane, that covers the entire macula (Figure 40–5). Embedded on the surface of this membrane are fine, dense particles of calcium carbonate called otoconia (“ear dust”), which give the otolith (“ear stone”) organs their name. Otoconia are typically 0.5 to 10µm long; millions of these particles are attached to the otolithic membranes of the utricle and saccule.

Figure 40–5 The utricle is organized to detect tilt of the head. Hair cells in the epithelium of the utricle have apical hair bundles that project into the otolithic membrane, a gelatinous material that is covered by millions of calcium carbonate particles (otoconia). The hair bundles are polarized but are oriented in different directions (see Figure 40–6). Thus when the head is tilted, the gravitational force on the otoconia bends each hair bundle in a particular direction. When the head is tilted in the direction of a hair cell’s axis of polarity, that cell depolarizes and excites the afferent fiber. When the head is tilted in the opposite direction, the same cell hyperpolarizes and inhibits the afferent fiber. (Adapted, with permission, from Iurato 1967.)

Gravity and other linear accelerations exert shear forces on the otoconial matrix and the gelatinous otolithic membrane, which can move relative to the membranous labyrinth. This results in a deflection of the hair bundles, altering activity in the vestibular nerve to signal linear acceleration owing to translational motion or gravity. The orientations of the otolith organs and the directional sensitivity of individual hair cells are such that a linear acceleration along any axis can be sensed. For example, with the head in its normal position, the macula of each utricle is approximately horizontal. Any substantial acceleration in the horizontal plane excites some hair cells in each utricle and inhibits others, according to their orientations (Figure 40–6).

Figure 40–6 The axis of mechanical sensitivity of each hair cell in the utricle is oriented toward the striola. The striola curves across the surface of the macula, resulting in a characteristic variation in the axes of mechanosensitivity (arrows) in the population of hair cells. Because of this arrangement, tilt in any direction depolarizes some cells and hyperpolarizes others, while having no effect on the remainder. (Adapted, with permission, from Spoendlin 1966.)

In some instances the vestibular input from a receptor may be ambiguous. For example, acceleration signals from the otolith organs do not distinguish between linear acceleration owing to translation and acceleration owing to gravity (Figure 40–7). The brain, however, integrates inputs from the semicircular canals, otolith organs, and visual and somatosensory systems to properly interpret head and body motions.

Figure 40–7 Vestibular inputs signalling body posture and motion can be ambiguous. The postural system cannot distinguish between tilt and linear acceleration of the body based on otolithic inputs alone. The same shearing force acting on vestibular hair cells can result from tilting of the head (left), which exposes the hair cells to a portion of the acceleration (a) owing to gravity (Fg), or from horizontal linear acceleration of the body (right).

The operation of the paired saccules resembles that of the utricles. The hair cells represent all possible orientations within the plane of each macula, but the maculae are oriented vertically in nearly parasagittal planes. The saccules are therefore especially sensitive to vertical accelerations including gravity. Certain saccular hair cells also respond to accelerations in the horizontal plane, in particular those along the anterior–posterior axis.

Most Movements Elicit Complex Patterns of Vestibular Stimulation

Although the actions of the vestibular organs may be separated conceptually and experimentally, actual human movements generally elicit a complex pattern of excitation and inhibition in several receptor organs in both labyrinths. Consider, for example, the act of leaving the driver’s seat of an automobile.

As you begin to swivel toward the door, both horizontal semicircular canals are stimulated strongly. The simultaneous lateral movement out the car’s door stimulates hair cells in both utricles in a pattern that changes continuously as the orientation of the turning head changes with respect to the direction of bodily movement. When rising to a standing position, the vertical acceleration excites an appropriately oriented complement of hair cells in each of the saccules while inhibiting an oppositely oriented group. Finally, the maneuver’s conclusion involves linear and angular accelerations opposite to those when you started to leave the car.